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A New Method for Quantifying Heterochrony in Evolutionary Lineages

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A New Method for Quantifying Heterochrony in Evolutionary Lineages Paleobiology, 47(2), 2021, pp. 363–384 DOI: 10.1017/pab.2020.17 Article A new method for quantifying heterochrony in evolutionary lineages James C. Lamsdell Abstract.—The occupation of new environments by evolutionary lineages is frequently associated with morphological changes. This covariation of ecotype and phenotype is expected due to the process of nat- ural selection, whereby environmental pressures lead to the proliferation of morphological variants that are a better fit for the prevailing abiotic conditions. One primary mechanism by which phenotypic variants are known to arise is through changes in the timing or duration of organismal development resulting in alterations to adult morphology, a process known as heterochrony. While numerous studies have demon- strated heterochronic trends in association with environmental gradients, few have done so within a phylogenetic context. Understanding species interrelationships is necessary to determine whether morphological change is due to heterochronic processes; however, research is hampered by the lack of a quantitative metric with which to assess the degree of heterochronic traits expressed within and among species. Here I present a new metric for quantifying heterochronic change, expressed as a hetero- chronic weighting, and apply it to xiphosuran chelicerates within a phylogenetic context to reveal con- certed independent heterochronic trends. These trends correlate with shifts in environmental occupation from marine to nonmarine habitats, resulting in a macroevolutionary ratchet. Critically, the distribution of heterochronic weightings among species shows evidence of being influenced by both historical, phylogenetic processes and external ecological pressures. Heterochronic weighting proves to be an effective method to quantify heterochronic trends within a phylogenetic framework and is readily applicable to any group of organisms that have well-defined morphological characteristics, ontogenetic information, and resolved internal relationships. James C. Lamsdell. Department of Geology and Geography, West Virginia University, Morgantown, West Virginia 26506, U.S.A. E-mail: [email protected] Accepted: 15 March 2020 Data available from the Dryad Digital Repository: https://doi.org/10.5061/dryad.pzgmsbcgp Introduction explosion (Erwin and Valentine 2013), invasion of freshwater ecosystems (Davis et al. 2018), Understanding the evolutionary patterns colonization of land (Benton 2010), and recov- and processes that drive the generation of ery from mass extinction events (Toljagić and new phenotypes and occupation of previously Butler 2013). In turn, the innovation of pheno- unexploited environments (the occurrence of types is recognized to occur through heritable novelty and innovation, sensu Erwin 2017)is alterations in the timing of an organism’sdevel- a fundamental goal of evolutionary study. opment, a process known as heterochrony The topic of novelty and innovation has most (McNamara and McKinney 2005;McNamara frequently been explored through the lens of 2012; Colangelo et al. 2019). Therefore, hetero- adaptive radiation (Losos 2010; Yoder et al. chronic processes result in new morphological 2010), which posits that ecological opportun- characteristics that can allow organisms to exploit ities combined with chance phenotypic evolu- new environments and subsequently diversify. tion permits exploration of new ecospace Natural biological systems are complex (Stroud and Losos 2016). This model of adap- entities, in which both environmental inter- tive radiation has been invoked as the domin- action and historical components are poten- ant causal factor of major evolutionary events tially equally important (Eldredge and Salthe in Earth’s history, including the Cambrian 1984; Vrba and Eldredge 1984; Erwin 2015b; © 2020 The Paleontological Society. This is an Open Access article, distributed under the terms of the Creative Commons Attribution licence (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted re-use, distribution, and reproduction in any medium, provided the original work is properly cited. 0094-8373/21 Downloaded from https://www.cambridge.org/core. IP address: 170.106.202.58, on 01 Oct 2021 at 16:50:49, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/pab.2020.17 364 JAMES C. LAMSDELL Lamsdell et al. 2017; Congreve et al. 2018). Evo- for each species within the analysis is devel- lutionary trajectories are defined by the inter- oped. Each character represents an aspect of action of two semi-independent genealogical morphology that may exhibit a paedomorphic, and ecological hierarchies (Eldredge and Salthe peramorphic, or neutral heterochronic expres- 1984; Congreve et al. 2018); as such, ecological sion. The peramorphic and paedomorphic con- changes have the potential to influence hetero- ditions for each character are determined based chronic processes to the same extent as hetero- on a ranked series of criteria: chronic changes might alter the potential for ecological occupation. Therefore, pluralistic 1. direct observations of ontogenetic changes approaches are required to determine the rela- within the target species; tive importance of ecological or evolutionary 2. ontogenetic changes observed in closely mechanisms behind biotic responses (Lamsdell related species; et al. 2017;Tuckeretal.2017;Congreveetal. 3. ontogenetic changes observed in extant 2018), representing a synthesis of macroevolu- relatives; tionary and macroecological topics and methods. 4. comparison with outgroup juvenile morph- Heterochrony, however, has rarely been stud- ology or ontogeny for character polarity; and ied within an explicitly phylogenetic context 5. comparison with outgroup adult morph- (Bardin et al. 2017). Cranial evolution of angui- ology for character polarity. morphan lizards (Bhullar 2012) and theropod dinosaurs (Bhullar et al. 2012) has been exam- Once the polarity of the morphology of hetero- ined by placing heterochronic changes within chronic expression for each character is estab- a phylogenetic hypothesis, but no attempt to lished, characters are coded for each species incorporate ecological occupation into such and assigned a score. A paedomorphic condi- investigations has been made. These studies tion is assigned a negative (−1) score, a pera- have also focused on only a subset of morpho- morphic condition is assigned a positive (+1) logical characters that may show heterochronic score, and a neutral condition is assigned a trends, which may obscure overall patterns of score of 0. If a character cannot be coded for a heterochrony within lineages, as traits display given species, either due to it not being pre- patterns of mosaic evolution (Hopkins and Lid- served or its condition being otherwise unclear, gard 2012;Huntetal.2015), whereby individual it is not given a score and does not contribute to traits may exhibit different modes of evolution the analysis. The total number of characters within a lineage. Recognizing overall hetero- within the matrix depends on the number of chronic trends within a lineage beyond the identifiable heterochronically influenced traits trajectories of individual traits is key to under- within a lineage; as such, organisms with standing the role of heterochrony in evolution. more complex morphologies and better- Furthermore, appropriate methods to quantita- understood ontogenies will result in larger het- tively compare heterochronic trends between erochronic matrices. A larger matrix allows for lineages have been lacking until now. Here, increased granularity in the heterochronic I use phylogenetic paleoecology to analyze pat- weighting, and ideally a matrix will comprise terns in ecological affinity and heterochronic 10 or more characters; however, it is possible trends across xiphosuran chelicerates and pre- to generate a heterochronic weighting for a sent a new metric for quantitatively representing taxon that has as few as three characters coded. heterochronic changes within an evolutionary Each of the characters coded for a species in lineage. the matrix contributes to the heterochronic weighting of the species, calculated as: Data and Methods n h = i=1 i ( ) — Hwj 1 Quantifying Heterochrony. Anovel n approach for quantifying heterochrony is pro- posed herein, whereby a character matrix com- where Hw is the heterochronic weighting of prising a series of multistate characters coded species j, derived from the mean of the Downloaded from https://www.cambridge.org/core. IP address: 170.106.202.58, on 01 Oct 2021 at 16:50:49, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/pab.2020.17 QUANTIFYING HETEROCHRONY IN XIPHOSURIDS 365 combined heterochronic scores (η)ofn charac- weights retrieved for a given clade are therefore ters, resulting in a value between 1.00 (more compared with a distribution of weight scores peramorphic) and −1.00 (more paedomorphic). over an identical topology; as such, rando- In turn, the heterochronic weighting of a given mized distributions should be generated for clade is calculated as: each topology used in an analysis. In this way, disparate analyses can determine whether clades fall within the tails of the expected het- N Hw []= j=1 j ( ) erochronic weighting distribution given their Hw k 2 N phylogenetic topology. Node- versus Tip-based Analyses.—Scores for where [Hw] is the heterochronic weighting of heterochronic weighting can be
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